Behavioral/Cognitive

Motor Commands Induce Time Compression for TactileStimuli

Alice Tomassini,1 Monica Gori,1 Gabriel Baud-Bovy,1,2 X Giulio Sandini,1 and Maria Concetta Morrone3,4

1Department of Robotics, Brain and Cognitive Sciences, Istituto Italiano di Tecnologia, 16163 Genova, Italy, 2Faculty of Psychology, Universita Vita-SaluteSan Raffaele, 20132 Milano, Italy, 3Department of Translational Research on New Technologies in Medicine and Surgery, Universita di Pisa, 56123 Pisa,Italy, and 4Scientific Institute Stella Maris, 56018 Calambrone, Pisa, Italy

Saccades cause compression of visual space around the saccadic target, and also a compression of time, both phenomena thought to berelated to the problem of maintaining saccadic stability (Morrone et al., 2005; Burr and Morrone, 2011). Interestingly, similar phenomenaoccur at the time of hand movements, when tactile stimuli are systematically mislocalized in the direction of the movement (Dassonville,1995; Watanabe et al., 2009). In this study, we measured whether hand movements also cause an alteration of the perceived timing oftactile signals. Human participants compared the temporal separation between two pairs of tactile taps while moving their right hand inresponse to an auditory cue. The first pair of tactile taps was presented at variable times with respect to movement with a fixed onsetasynchrony of 150 ms. Two seconds after test presentation, when the hand was stationary, the second pair of taps was delivered with avariable temporal separation. Tactile stimuli could be delivered to either the right moving or left stationary hand. When the tactile stimuliwere presented to the motor effector just before and during movement, their perceived temporal separation was reduced. The timecompression was effector-specific, as perceived time was veridical for the left stationary hand. The results indicate that time intervals arecompressed around the time of hand movements. As for vision, the mislocalizations of time and space for touch stimuli may be conse-quences of a mechanism attempting to achieve perceptual stability during tactile exploration of objects, suggesting common strategieswithin different sensorimotor systems.

Key words: action; sensory-motor; time perception; touch

IntroductionThe external world is mainly sensed through active exploration(Gibson, 1962), and awareness of one’s own movement is funda-mental to attribute sensory stimulation to its true physical source(Helmholtz, 1866).

In recent years the inherent interdependence between sensoryand motor functions has been recognized as a general and indis-putable operating principle in the brain, extending the notion of“purely sensory” to encompass also the implicit role of motorsignals: meaningful information about the spatial and temporalarrangement of events in the external world cannot be gainedunless sensory information is integrated with a representation ofone’s own body and its movement (Vaziri et al., 2006; Rucci et al.,2007; Medendorp, 2011; Yoshioka et al., 2011). The haptic senseis an exemplar case of sensory-motor integrative processes. Tac-tile events uniquely occur on the body surface and most often asa result of an active movement of the body. To accurately locate

tactile events in space and time somatotopic codes must be dy-namically updated through integration with proprioceptive andmotor information. Internally generated action-signals mightprovide predictions about the location of the stimulated body sitein space as well as about the timing of stimulation allowing tocoping with delays and variability in sensory transmission. How-ever, a temporal mismatch between the prediction and the actualmovement could cause perceptual alterations that have been ob-served in both vision and touch.

Visual stimuli flashed just before and during the execution ofsaccades are mislocalized toward the saccadic target, inducing defacto a compression of space along the direction of the movement(Morrone et al., 1997; Ross et al., 1997; Lappe et al., 2000). Com-plex distortions affect not only space but also time, and do so witha similar time course tightly locked to eye movement execution(Morrone et al., 2005; Binda et al., 2009). Apparent event time isboth shifted and compressed so that the temporal separation oftwo visual stimuli is reduced by half of its physical length andeven their order of appearance sometimes reversed.

These findings are thought to be interconnected and be theexpression of a predictive mechanism, grounded on interlacedrepresentations of space and time, that probably absolves thecomplex role of visual perceptual stability (Burr and Morrone,2011). Distortions of time are also linked to the internal bodyschema representation and can be so strong to induce a reversalin the apparent order of tactile events (Yamamoto and Ki-

Received July 1, 2013; revised May 26, 2014; accepted May 31, 2014.Author contributions: A.T., M.G., G.B.-B., G.S., and M.C.M. designed research; A.T. performed research; A.T. and

G.B.-B. analyzed data; A.T. and M.C.M. wrote the paper.This work was supported by PF7-EC projects XPERIENCE, ERC-STANIB, and ERC-ECSPLAIN. We thank Marco

Jacono for his help in building the setup and preparing the experiments.The authors declare no competing financial interests.Correspondence should be addressed to Dr Alice Tomassini, Department of Robotics, Brain and Cognitive Sciences

(RBCS), Istituto Italiano di Tecnologia (IIT), Via Morego 30, 16163 Genova, Italy. E-mail: alice.tomassini@iit.it.DOI:10.1523/JNEUROSCI.2782-13.2014

Copyright © 2014 the authors 0270-6474/14/349164-09$15.00/0

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tazawa, 2001a,b), similarly to what has been shown for perisac-cadic vision (Binda et al., 2009).

Interestingly, some data suggest that similar phenomena alsooccur around the time of hand movements, when tactile stimuliare systematically mislocalized in the direction of the movement(Dassonville, 1995; Watanabe et al., 2009; Maij et al., 2011) andperceptually delayed with respect to the subjective onset time ofthe movement (Dassonville, 1995; Jackson et al., 2011). This sug-gests that similar strategies may be exploited by different sensorimotorsystems during the active exploration of the environment.

In this study, we adopted a paradigm similar to that previouslyused in vision (Morrone et al., 2005) and measured whether handmovements cause an alteration of the perceived timing of tactilesignals.

Materials and MethodsApparatusParticipants sat in front of a table with both hands resting on two hand-shaped plaster casts. The cast for the right hand was mounted on a slidingguide (length, 1.5 m) so that its movement was constrained along onedirection.

Tactile stimulations were delivered by means of two solenoid tappers (di-ameter 8 mm, weight 2 g; MST3 Miniature Solenoid Tappers, M&E Solve)securely fixed on the right and left index finger pads with a Velcro strap.

The movement of the right hand was recorded by means of motiontracking cameras (Optotrak Certus Motion Capture System, Northern

Digital) that measured the position of onemarker, attached to the nail of the right indexfinger, at a sampling rate of 200 Hz.

To determine the time instant when the tac-tile stimulations were presented relative to themovement of the hand, a third tapper was op-erated in synchrony with the stimulating tap-pers and the movement of its pin was alsorecorded by the Optotrak system and used as atime stamp.

Forces and torques produced by the righthand were also measured by a six-axis force/torque transducer (Mini40 F/T transducer;ATI Industrial Automation) fixed to the lowersurface of the plaster cast.

ProcedureExperiment 1: temporal judgments during move-ment. Participants were asked to compare thetemporal separation between two pairs of tac-tile taps while performing rapid movementswith their right arm. An auditory tone (fre-quency 440 Hz; duration 50 ms) marked thebeginning of each trial. After a variable interval(ranging from 0.8 to 1.8 s) a second, identicalauditory tone cued participants to move theirright hand as fast as possible. At variable delaysfrom the sound presentation (from �0 to�700 ms after the sound) the first pair of taps(the test) was delivered to the right/left indexfinger with a fixed temporal separation of 150ms. Two seconds after the test presentation thesecond pair of taps (the probe) was delivered tothe same hand, with a variable separation rang-ing from 50 to 250 ms (Fig. 1A; schematic illus-tration of the experimental paradigm). Theintensity of each tactile tap was 2.5 V (corre-sponding to a peak force of 27.5 g as measuredwith a precision scale) and its duration 8 ms.To check that the actual stimulus timing corre-sponded to that commanded via computer werecorded the time course of the pin displace-ment by means of an analogic accelerometer

(attached on top of the tapper surface) at a sampling rate of 5000 Hz. Thetiming of the recorded acceleration profile matched the nominal stimu-lus timing (8 ms). Participants indicated verbally which pair of taps wasseparated by the longer time interval. Participants were required to keeptheir eyes closed and to wear noise-reducing headphones and earplugsthat according to the self-reports of all subjects were sufficient to maskthe noise produced by the tactile stimulators without preventing fromhearing the acoustic signals.

Before performing the experiment participants underwent a trainingphase during which they learned to execute rightward hand movementsof �450 ms in duration and 15 cm in amplitude in response to theauditory “go” signal. Approximately 20 hand movements were sufficientfor all participants to achieve a stable performance during training. Thepractice trials were also used to evaluate the subject’s mean reaction timeto appropriately set the presentation times of the test stimulus so thatsampling was mostly concentrated in a temporal window comprisedbetween 200 ms before to 200 ms after movement onset time.

Hand movements were checked on a trial-by-trial basis by the ex-perimenter and trials were discarded in case of incorrect movementexecution; an automated procedure also rejected trials when the re-action time and movement duration were �50 and 150 ms, respec-tively. To control the detectability of both taps in the test pair, weasked subjects to report whether they perceived one or two stimuli ineach trial and discarded all trials where unclear percepts occurred.Overall, the number of rejected trials did not exceed 3% for eachsubject and condition.

Figure 1. Experimental paradigm and conditions. A, Schematic representation of the movement of the hand and of the relevantsensory events occurring during each trial: all events are aligned in time. Each trial starts with the presentation of an acoustic tone(start signal); after a variable pause a second tone is presented (go signal) that instructs participants to move their right hand as fastas possible. The first pair of tactile taps (test) is presented at variable delays from the go signal, with a fixed onset asynchrony of 150ms. After 2 s from test presentation the second pair of taps is presented (probe) with a variable temporal separation. B, Experi-mental conditions. The movement condition implies the movement of the right hand; tactile stimulations are delivered either tothe right moving hand or to the left static hand with equal probability across trials. The isometric contraction condition implies thegeneration of a transient lateral force against a block, with no movement execution; tactile stimulation is always delivered to theright contracting hand.

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We tested two different conditions (Fig. 1B):the movement condition where participantswere required to move their right arm and theisometric contraction condition where partici-pants produced a horizontal force with theirright arm with actual displacement impeded bya block. In the movement condition, the twopairs of tactile taps were both presented ran-domly to the right or to the left index fingerwith equal probability of stimulating eitherhand while in the isometric contraction condi-tion tactile stimuli were always delivered to theright index finger.

Data were collected on eight participants(mean age � 26.28 � 1.5 years; two males; oneauthor). Seven subjects were tested on themovement condition. Three subjects from theprevious group plus one author performed alsothe isometric contraction condition. All sub-jects completed at least 16 sessions for themovement and seven sessions for the isometriccontraction condition of 60 trials each.

Experiment 2: control for tactile suppression.To control for the effects of tactile suppressionduring movement on perceived time we per-formed an intensity-matching experiment.First, we measured the amount of tactile atten-uation during movement. Each stimulus con-sisted in a single tactile tap, instead of a pair oftaps; the test stimulus, delivered just before orduring movement, had fixed intensity of 2.5 V(equal to the intensity of the stimuli used inExperiment 1), whereas the probe, delivered after the movement whenthe hand was stationary again, varied in intensity on a trial-by-trial basis(from 1.4 to 3 V). Subjects had to report verbally which of the two stimuliwas perceived as more intense. We then repeated the time perceptionexperiment in stationary conditions (with neither hand movementnor contraction) manipulating the intensity of the stimuli deliveredto the right resting hand according to the results obtained in the abovedescribed intensity-matching condition. Two conditions were ran-domly intermingled: in the baseline condition, the test stimulus (150ms) and the probe (variable temporal separation) had the same phys-ical intensity of 2.5 V; in the matched condition, the probe always hadan intensity of 2.5 V, whereas the intensity of the test was matched,separately for each subject, to the lowest intensity perceived duringmovement. We tested five of the seven naive subjects who had alreadytaken part in Experiment 1.

Given the objective two-alternative forced choice design (2AFC), weplanned five subjects for each experiment and condition. Unfortunately,only three participants of the original group (Experiment 1) gave theiravailability to complete also the isometric contraction condition. Thus,we decided to include one of the authors (A.T.) for this condition. Toallow for the appropriate within-subject comparisons the author com-pleted both the movement (with stimuli delivered only to the movinghand) and the isometric condition.

Data analysisData analysis was performed off-line. Movement onset time was deter-mined by an automated algorithm as the instant corresponding to thefifth frame of a series of 10 consecutive frames where the first derivative ofthe velocity of the hand was greater than zero. The same computation wasapplied to the force produced along the axis parallel to the direction ofthe movement to yield force onset time. This force component was cho-sen as it was aligned with the direction along which the participantspushed. The end of the movement was determined as the instant of timewhen hand velocity became �10 mm/s.

The time of stimulus presentation with respect to hand movement wasdetermined by applying a velocity threshold (15 mm/s) to the movementof the tapper triggered in synchrony with the first tap of the test pair and

recorded by the Optotrak system. The time of stimulus presentation withrespect to hand force was determined by acquiring jointly the voltagesignal delivered to the tapper controller and the data from the forcesensor by means of a national instrument data acquisition device (sam-pling rate 1000 Hz). Test presentation times were then expressed relativeto the central point of the temporal interval (150 ms) marked by the testpair. Stimulus latencies were calculated as the difference between testpresentation time and movement (for the movement condition) or force(for the isometric contraction condition and for the intensity-matchingcontrol experiment) onset time. Thus, negative and positive latency val-ues indicate that the center of the test interval fell before and after theonset of hand movement/contraction, respectively.

Data were grouped in different bins according to stimulus latency andthen fitted separately with cumulative Gaussian functions, estimated bymeans of the Maximum Likelihood method. Bin size was chosen so thatpsychometric functions were never fitted to datasets with �30 trials.Approximately 50 trials served on average to calculate each psychometricfunction.

Both the Point of Subjective Equality (PSE) and the Just NoticeableDifference threshold [corresponding to the standard deviation (SD) ofthe fitted cumulative Gaussian function] were derived from the psycho-metric function parameters. The standard errors (SEs) of the PSEs andSDs were estimated by bootstrap.

The above described analysis requires a minimum number of trials(�30) to have reliable fitting of the psychometric functions, constrainingthe size and position of the latency bins.

To be able to evaluate on statistical basis the relation between per-ceived time (PSE) and stimulus latency taking into account the differentnumber of trials collected for each subject and stimulus presentationtime we analyzed the pool of single trials using the powerful generalizedlinear mixed model (GLMM) analysis (Moscatelli et al., 2012). TheGLMM analysis was conducted after data collection for the entire subjectpool was completed. We applied GLMM with a logit link function and aBernoulli distribution. With this analysis, a single model is fitted for allsubjects, taking into account the individual variability in the responsesand the different number of observations (trials) collected for each sub-ject. To keep complexity at a reasonable level, separate GLMM analyseswere conducted for the moving and stationary hand including the whole

Figure 2. Psychometric functions showing the proportion of trials where the probe was judged to be longer than the test. Datafor two representative subjects (SC and LD) are shown for three different stimulus presentation times relative to movement onset(�170,�40 and�40 ms; bin size of 80 ms) when the test was either delivered to the right moving (black) or left stationary (lightgray) hand.

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set of trials with stimulus latencies up to 400 ms before movement onset.The model included probe (stimulus temporal separation, probeij forsubject i and trial j) and latency (latij) as fixed effects and subject andprobe as random factors as follows:

Yij � �0 � ui0 � ��1 � ui1 probeij � �2latij (1)

where Yij denotes the response variable, b0, b1, and b2 represent thefixed-effect parameters of the model, and ui0 and ui1 represent the ran-

dom component of the overall variability. Therandom factors (ui0 and ui1 in Eq. 1) were se-lected by comparing various covariance struc-tures and choosing the model with the lowestAkaike Information Criterion, which takesinto account the goodness of fit and the num-ber of parameters (the complexity) of themodel.

ResultsExperiment 1: time compression duringmovementData for two representative subjects areshown in Figure 2 for three critical stimu-lus presentation times relative to handmovement onset. The temporal intervalestimation varies whether the stimulus ispresented long before, close or duringmovement execution and whether on themoving or on the stationary hand. Wellbefore movement initiation (�170 ms;Fig. 2, left), time perception is almost ac-curate for stimuli presented to eitherhand. The fitted psychometric functionsfrom the moving and static hands arenearly overlapped, with PSEs approachingthe actual time interval (150 ms) in bothcases. When the tactile taps are presentedto the right moving hand close to move-ment onset (�40 ms; Fig. 2, middle), theirapparent temporal separation is reducedby �30 ms, yielding PSEs of 121 � 4 ms(SE) and 124 � 3 ms (SE) for subjects SCand LD, respectively. A similar compres-sion of time is observed when the stimuliare presented just after the movement hasstarted (�40 ms; Fig. 2, right).

We find that for all participants per-ceived duration in the epoch shortlypreceding (�50 ms) and following move-ment onset (� 50 ms) is very differentbetween the two hands (Fig. 3A). All PSEsfor the moving hand are �150 ms,whereas they are clustered �150 ms forthe static hand. In other words, perceivedtime is compressed for the right movinghand while almost veridical for the leftstationary hand. Importantly, we also findthat the task is performed with the sameprecision (SD) for both hands, notwith-standing whether time is compressed orveridical (Fig. 3B), indicating that move-ment preparation and execution do notimpair temporal judgments.

The PSEs averaged over the temporalwindow between �100 and � 100 ms are

significantly different for the moving and static hands (t(6) ��4.177, p � 0.006; two-tailed paired-samples t test) with a 13%of reduction in apparent time for the right hand (t(6) � �7.246,p � 0.0001, two-tailed one-sample t test, H0: � � 150 ms) andvirtually veridical time for the left hand (t(6) � 0.320, p � 0.759;two-tailed one-sample t test, H0: � � 150 ms; Fig. 3C, left). How-ever, the precision thresholds do not significantly differ between

Figure 3. Individual PSEs (A) and SDs (B) for stimuli delivered to the right hand are plotted against those for stimuli deliveredto the left hand when the center of the test interval fell within 100 ms before movement onset (latency �50 ms; left) and 100 msafter movement onset (latency �50 ms; right). The diagonals show equal perceived time (A) and precision in temporal judgments(B) for the two hands. The vertical and horizontal dashed lines (A) indicate physical durations. The black and light gray arrows showthe means for the right and left hand, respectively; results for all subjects. Error bars represent SEM. C, Average PSEs (left) and SDs(right) for the moving and stationary hand over stimulus latencies comprised between �100 and �100 ms. The horizontaldashed line (left) indicates physical test duration. Error bars represent SEM.

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the moving and stationary hand (t(6) � �0.609, p � 0.565; two-tailed paired-samples t test), being �30 ms on average (Fig. 3C,right).

To investigate the temporal dynamics of the time compressioneffect, we took advantage of the existing variability in stimuluslatency, defined as the time between the center of the test intervaland movement onset (the average latencies � SD ranged from�24 � 197 ms to 285 � 350 ms depending on the individualreaction times). First, we considered a latency window comprisedbetween �200 ms and �200 ms. We grouped data in five binscentered on �167, �100, �33, 50, 150 ms so that each bin con-tained at least 30 trials for each subject and hand. Figure 4 showsthe across-subjects average of the PSEs for each hand and bin. Atwo-way repeated-measures ANOVA on the PSEs with hand andlatency as factors confirmed that time intervals appear shorter forthe moving compared with the static hand (F(1,6) � 16.666, p �0.006; main effect of factor hand). This analysis yielded also amarginally significant interaction between factor hand and la-tency (F(4,24) � 2.624, p � 0.06) reflecting the observation that

perceived time for the right hand shows the tendency to shortenas the time of movement approaches (Fig. 4A). A seemingly op-posite trend is observed for the left hand. However, the variationover time of the mean PSEs for the stationary hand is mainly dueto the results of one subject (Fig. 4B), as indicated by the verylarge associated errors. The differential temporal modulation ofthe effect for the moving and stationary hand is confirmed byfurther analysis. Given the great variability in the individual re-action times, we could not average the results across subjects forstimulus latencies earlier than �170 ms relative to movementonset. To deal with the individual variation in dynamics, we com-pared the PSEs at the earliest stimulus latencies for each subject(that varied depending on the individual reaction times) with thePSEs around movement onset. Figure 4B shows the change inperceived duration in trials corresponding to the earliest latenciesobserved for each subject (average � SD latencies varied from�239 � 28 ms to �142 � 29 ms depending on the subject; grandaverage � SD � �216 � 21 ms) against the compression occur-ring around movement onset (grand average � SD latency �35 � 8 ms) for the two hands. The pattern of results for the twohands is strikingly different. The data for the moving hand (blacksquares), with only one exception, are gathered below the equal-ity line (diagonal) indicating a progressive reduction in perceivedtime during the motor preparatory period. On the contrary, thedata for the stationary hand lie on the equality line indicating nochange in perceived time as a function of stimulus latency. Thetwo-way ANOVA for repeated measures with hand and latency(two latency bins; Fig. 4B) as within-subject factors confirmedthe significant difference in perceived time between the twohands (F(1,6) � 17.767, p � 0.006) and most importantly yieldeda significant interaction between hand and latency (F(1,6) �9.396, p � 0.022). Moreover, to analyze the time course of theeffect without binning the data we performed separate GLMManalyses for the moving and stationary hand including all trialswith stimulus latencies up to 400 ms before movement onset (seeMaterials and Methods). For the right moving hand, we found astatistically significant effect for the factors probe (b0 � 0.0622,p � 0.0001) and latency (b1 � 0.0023, p � 0.03). The positive signof the coefficient for the latency factor indicates that apparenttime progressively shortens as stimulus presentation time ap-proaches the onset of the hand movement. No significant effect oflatency was found for the left stationary hand (b0 � 0.0636, p �

Figure 4. A, Average PSEs as a function of stimulus presentation time. The dashed horizontalline indicates physical duration; the dashed vertical line indicates movement onset time. Errorbars represent SEM. B, PSEs around movement onset time (average � SD latency � 35 � 8ms) plotted against those early before movement (average � SD latency � �216 � 21 ms)for the moving (black) and stationary hand (light gray; results for all subjects). The PSEs earlybefore movement were calculated on the 60 trials with the earliest stimulus presentation timescollected for each subject (starting from �300 ms), whereas the PSEs around movement onsetincluded 60 trials up to stimulus latencies of 75 ms. The vertical and horizontal dashed linerepresents physical duration. The diagonal shows equal perceived time early before and aroundmovement onset. Error bars represent SEM.

Figure 5. Average PSEs for stimuli presented to the moving and stationary hand as a func-tion of stimulus presentation time, when fast and slow hand movements were executed. Thedashed horizontal line indicates veridical duration; the dashed vertical line indicates movementonset time. Error bars represent SEM. The star represents statistical significance (� � 0.05) ofthe difference between PSEs for fast and slow movements when the center of the test intervalsfell within �75 and 0 ms (relative to movement onset).

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0.0001 and b1��0.0013, p � 0.212 for the probe and latency factorsrespectively), indicating that time compression is not due to motorpreparation per se but it is specific for the motor effector.

The amplitude and duration of the arm movements per-formed by the participants during the experiment were 17 � 1 cmand 498 � 23 ms on average, which matched reasonably well therequirements. Arm velocity profiles were bell-shaped with peakvelocity of 603 � 22 mm/s reached �230 � 9 ms on average(mean � SE). Although rather small, we exploited the across-trialvariability in the movement kinematics to test whether the timecompression effect is influenced by some characteristics of themovement. Individual data were analyzed separately dependingon whether movement velocity was higher or lower than themedian of the velocity distribution for each latency bin in themost critical time window (from �150 to �150 ms).

Average PSEs are reported in Figure 5 for the moving andstationary hands. Interestingly, faster movements caused a stron-ger compression of time for the stimuli delivered to the movinghand, only in the short moment just preceding movement onset(��40 ms; t(6) � 3.005, p � 0.024; two-tailed paired-samples ttest) when a difference in velocity between the two datasets wasnot reached yet (t(6) � �1.778, p � 0.126; two-tailed paired-samples t test), pointing to an influence of the preparation formovement. No other significant difference was reported betweenfast and slow movements for either the moving or the static hand.

To understand the nature of the motor signals that may causethe observed temporal distortion we tested a further condition inwhich no movement was executed, but subjects were asked toproduce a transient force against a block. The pattern of resultsobtained when subjects simply contracted hand muscles closelymirrors that obtained when they actually moved their hand. PSEsfor the four tested subjects are shown in Figure 6 as a function of

stimulus latency relative to force onsettime. Regardless of the individual differ-ences in the strength and time course ofthe effect, all subjects show a similar re-duction in perceived time with similartemporal dynamics in the condition ofreal movement compared with the condi-tion of isometric contraction. A 2 4ANOVA for repeated measures was con-ducted on the PSE data with movement(movement vs isometric contraction) andlatency (two latency bins before and afterforce onset) as within-subjects factorsyielding no significant main effect of fac-tor movement (F(1,3) � 1.28, p � 0.34) aswell as no significant interaction effect(F(3,9) � 2.14, p � 0.165).

Experiment 2: effect of tactilesuppression on perceived timeBody movement as well as isometric con-traction is known to be preceded and ac-companied by a transient damping intactile sensitivity which is generally re-ferred to as tactile suppression (Williamset al., 1998). There is also evidence thattemporal judgments are affected by thestrength of sensory stimulation (for ex-ample, by visual contrast and luminance),with weaker and masked stimuli appear-ing shorter (Terao et al., 2008). In Exper-

iment 1 to control the detectability of both taps in the pair, weasked subjects to indicate whether they perceived one or twostimuli in each trial. The overall number of trials where unclearpercepts were reported was very low (�1%) and they were dis-carded from analysis. In addition, to be sure that any effect onperceived time observed during movement was not a mere con-sequence of tactile suppression, we performed a control experi-ment on five of the seven naive subjects who had taken part in themain experiment. First, we measured the amount of reduction inthe perceived intensity of tactile stimuli delivered to the motoreffector at different times with respect to the movement (from�200 ms before to �100 ms after force onset time). The experi-mental procedure was identical to the Experiment 1 (movementcondition), except that subjects had to compare the perceivedintensity of the tactile stimulations. The intensity-matching ex-periment yields a similar pattern of results for all the five testedsubjects. In agreement with previous reports (Williams andChapman, 2000), perceived stimulus intensity on the hand effec-tor is attenuated both before and during movement. The attenu-ation effect gradually increases within the temporal windowinvestigated, reaching its maximal value for stimulus latencies of�0 –100 ms after force onset time (PSE � 1.8 � 0.1 V on average;Fig. 7A). Test stimuli of intensity values corresponding to theindividual PSEs obtained in the matching experiment for the0 –100 ms stimulus latencies (matched condition; see Materialsand Methods), intermingled with stimuli of standard intensity(baseline condition), were used in the temporal control experi-ment and delivered to the right stationary hand. Data for tworepresentative subjects (same subjects reported in Fig. 2) are plot-ted in Figure 7C, showing no difference in apparent time betweenthe matched and the baseline condition, as indicated by the nearlyoverlapping psychometric functions, and strong compression of

Figure 6. Individual PSEs for the movement and isometric contraction condition as a function of stimulus presentation timerelative to force onset time. The dashed horizontal line indicates physical test duration; the dashed vertical line indicates force onsettime. Error bars represent SEM.

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time for the movement condition. Tempo-ral judgments between the matched andbaseline condition were not significantlydifferent (t(4) � �1.038, p � 0.358; two-tailed paired-samples t test), whereas per-ceived time during movement (resultsfrom Experiment 1) is significantly re-duced with respect to the matched (t(4) �3.056, p � 0.038; two-tailed paired-samples t test; Fig. 7B), as well as to thebaseline condition (t(4) � �7.776, p �0.001; two-tailed paired-samples t test).We conclude that the reduction in per-ceived tactile intensity during movementcannot account for the reduction in per-ceived duration. The lack of difference be-tween the baseline and the matchedcondition further supports the conclusionthat the amount of tactile attenuationduring movement (at least for the stimu-lus intensities used in our study) is notsufficient to induce any significant bias inapparent time.

DiscussionWe show that time intervals marked bytactile stimuli appear shorter when handmovements are prepared and executed.Our result corroborates recent evidence ofa tight link between time perception andaction (Yarrow et al., 2001; Haggard et al.,2002; Morrone et al., 2005; Hagura et al.,2012; Tomassini et al., 2012) and shows aselective and anticipatory movement-related distortion of time. Critically, at themoments around action initiation, timecompression is restricted to the motor ef-fector. Duration is misjudged only when tactile stimuli are deliv-ered to the hand that is about to move and not when delivered tothe other, stationary hand, indicating that movement prepara-tion selectively disrupts temporal processing on the motoreffector.

Attention is known to exert powerful effects on time percep-tion (Tse et al., 2004), typically causing temporal expansion whenfocused on the timing task and contraction when directed else-where. There are many ways by which attentional factors mightinfluence duration judgments in our task but some of them canbe dismissed very easily. The compression of time cannot becaused by a general decrease of attention due to the dual-taskperformance (Fraisse, 1984; Brown, 1985). In fact, that wouldproduce comparable effects for the moving and stationary hand(as participants were equally engaged in the same attentional-demanding task) rather than selective effects, as we found. Timecompression cannot be due to a stronger attentional allocation tothe motor effector (Forster and Eimer, 2007), given that salientand attended stimuli generate expansion not compression oftime (Block and Zakay, 1997; Tse et al., 2004). Eye and handmovements have been shown to be coupled with predictive shiftsof attention to the movement target and to the motor effector(Eimer et al., 2006; Juravle and Deubel, 2009). However, oureffect is in the opposite direction from what is expected on thebasis of selective attention. Expansion, rather than compression,would be predicted for the stimuli delivered to the moving hand

if the change in apparent time was driven by a motor-related shift ofattention toward the effector. Moreover, tactile stimulations oc-curred with equal probability on either hand, ruling out any sys-tematic bias in somatosensory attention or prior-entry likeeffects. Therefore, we could exclude that the time compressionmerely reflects dynamic allocation of motor or spatial attention.Finally, time compression is unlikely to be ascribed to an unspe-cific increase in noise, owing for example to movement-inducedmasking effects, given that we observed the same precision intemporal judgments for the various conditions.

A general decrease in tactile sensitivity is known to occur earlybefore and during voluntary executed movements (Angel andMalenka, 1982; Milne et al., 1988; Williams et al., 1998; Shergill etal., 2003). This phenomenon, known as tactile suppression, hasprobably a central component, as it precedes movement onsetand even electromyographic activity (Williams et al., 1998). In-deed, it has been recently argued that time underestimationmight result from weak responses to transient signals, at least inthe visual system (Terao et al., 2008). We quantified the amountof tactile attenuation during movement and then measured per-ceived time in static conditions for stimuli whose physical inten-sity matched the perceived intensity during movement. Theresults indicate that apparent time for these low-intensitymatched stimuli is virtually veridical. Thus, the compression oftime observed is most likely a genuine movement-related effectand not simply a byproduct of suppression. However, in the pres-

Figure 7. Control experiment A, Average PSEs for the intensity-matching experiment plotted as a function of stimulus presen-tation time with respect to hand force onset. B, Average PSEs for the movement (results from the main experiment, black) and theintensity-matched condition (gray). The PSEs for the movement condition have been calculated in the same latency bin (0 –100 msafter force onset) that was used to determine the matching-intensity and then averaged across the same five subjects who tookpart in the control experiment. The dashed horizontal line indicates physical duration (150 ms). Error bars represent SEM. C,Psychometric functions showing the proportion of trials where the probe was judged to be longer than the test in the movement(black), intensity-matched (gray), and baseline (light gray) condition. Data for two representative subjects (SC and LD; samesubjects of Fig. 2) are shown.

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ent study we did not measure time compression during move-ment for stimuli of different intensities and uncontrolled ordereffects or learning may have influenced our results. Thus, becausenot all of the methodological decisions underlying this work werefinalized before the processes of data collection and analysis, ourfindings will benefit from confirmatory replication.

A growing number of evidence shows a close relation betweenmotor and temporal processing. Within the large and complexnetwork of areas that has been related to timing processes,“purely” motor circuits are indeed primarily represented (Lewisand Miall, 2003; Coull et al., 2004; Macar et al., 2006; Teki et al.,2011; Bueti et al., 2012; Coull et al., 2012). We find that theamount of time compression during motor preparation is mod-ulated by the velocity of the forthcoming movement, with greatercompression associated with preparation for faster movements.This suggests that high speed does not act by simply increasingthe noise level in reafferent signals transmission possibly enhanc-ing masking effects, as this would affect temporal judgments dur-ing motor execution rather than during preparation when theeffector is still stationary. Similarly, the modulation by move-ment speed is also unlikely to be ascribed to suppression, giventhat tactile suppression is not sufficient to induce the perceivedtime compression. Rather, this result is a strong indication thatthe motor preparatory activity may play a direct role in the tem-poral effects reported here. Indeed, it has been shown that thevelocity of upcoming movements is codified by the preparatorymotor activity of neurons in both premotor (PMd) and primarymotor areas (M1; Churchland et al., 2006). Not surprisingly, alsothe saccade-related effects on visual time are similarly modulatedby eye movement velocity (Ostendorf et al., 2007), outlining fur-ther connections between the visual and tactile phenomena.

To understand better the nature and origin of the temporaldistortion accompanying hand movements we tested also an iso-metric condition where motor processing should be free of anyspatial transformation that serves the construction of a motorplan. Our results show that motor efference, with no associatedspatial displacement of any body part, induces comparable com-pression of perceived time as actual movement. This suggests thatthe perceptual effects on time might be mediated by descendingmotor signals and not by ascending reafferent signals, which arelargely minimized in the isometric contraction condition. It alsoindicates that the motor signal responsible for these effects ismost probably a high-level signal in the motor hierarchy, gener-ated at an initial stage of motor processing when the intention-to-move is formulated. The haptic system provides an exclusiveopportunity to test whether the displacement of the body is anecessary condition to induce the perceptual distortions. Previ-ous studies have exploited this possibility investigating the tactilesuppression and obtaining similar results during contraction andmovement execution (Post et al., 1994; Williams and Chapman,2002; Wasaka et al., 2005). Thus, both compression and suppres-sion can take place without actual displacement of the body andboth precede movement onset. The two phenomena show evi-dent commonalities suggesting they might distinctively contrib-ute to a similar brain function.

The changes in apparent time that we observe for tactile stim-uli presented at the time of hand movements closely resemble theperisaccadic distortions of visual time. Several similarities can betraced between the two phenomena: for both modalities, the dis-tortion has an anticipatory nature, preceding movement onset,and it is modality- or effector-specific. The compression of tactiletime that we report differs however in some respects from itssaccadic counterpart. It is in fact smaller and has a slower tempo-

ral dynamics. Apparent visual time is reduced up to half of itsphysical length starting from �150 ms before saccadic onset,whereas the decrease in tactile time begins slightly earlier (� 200ms, although with some variation across subjects) and reaches amaximum of 15%. The faster dynamics of the visual effect mightreflect the faster time course of the motor preparatory activitywithin the oculomotor system. Another phenomenon commonto the visual and tactile domain is the apparent temporal inver-sion of two separate stimuli that take place during the planning ofhand (Hermosillo et al., 2011) and eye movements (Morrone etal., 2005; Kitazawa et al., 2008). Time order judgments are alsosusceptible to hand posture and body schema manipulations,implying that time alterations are dependent on spatial represen-tations (Morrone et al., 2010) built up through multimodal pro-cesses that order the flow of sensory events in time (Kitazawa etal., 2008).

The perisaccadic changes in visual time have been linked tothe mechanisms that achieve visual stability against the abruptshift of the retinal image consequent to eye movement (Binda etal., 2009; Burr and Morrone, 2011; Cicchini et al., 2013), proba-bly mediated by the predictive remapping of visual receptivefields (Duhamel et al., 1992; Sommer and Wurtz, 2002). Tactileinformation must be also remapped across hand movements (orskin somatotopy) to determine the position and shape of thetouched objects. As we move our hands, the relevant tactile fea-tures of the explored surfaces (e.g., edges, bumps, and dips) willsuccessively stimulate different portions of the skin (for exampledifferent fingertips). To correctly interpret this time-varying sig-nal and accurately reconstruct the object properties, informationabout the upcoming movements must be available. This knowl-edge might be used in advance both to filter out irrelevant signalsfrom the incoming sensory flow, as well as to appropriately re-map tactile signals across movements.

The compression of apparent time and the suppression mightthus reflect a complex and multifaceted set of mechanisms thatoptimize sensory-motor functions.

Whether the distortions of time and space for tactile stimuli atthe moment of action (Dassonville, 1995; Watanabe et al., 2009)share a common origin, as it has been suggested for vision, isan intriguing still open question. The present results mightsuggest a common strategy within different sensory-motordomains that may serve the maintenance of perceptual stabil-ity during movement.

ReferencesAngel RW, Malenka RC (1982) Velocity-dependent suppression of cutane-

ous sensitivity during movement. Exp Neurol 77:266 –274. CrossRefMedline

Binda P, Cicchini GM, Burr DC, Morrone MC (2009) Spatiotemporal dis-tortions of visual perception at the time of saccades. J Neurosci 29:13147–13157. CrossRef Medline

Block RA, Zakay D (1997) Prospective and retrospective duration judg-ments: a meta-analytic review. Psychon Bull Rev 4:184 –197. CrossRefMedline

Brown SW (1985) Time perception and attention: the effects of prospectiveversus retrospective paradigms and task demands on perceived duration.Perception and psychophysics 38:115–124. CrossRef Medline

Bueti D, Lasaponara S, Cercignani M, Macaluso E (2012) Learning abouttime: plastic changes and interindividual brain differences. Neuron 75:725–737. CrossRef Medline

Burr DC, Morrone MC (2011) Spatiotopic coding and remapping in hu-mans. Philos Trans R Soc Lond B Biol Sci 366:504 –515. CrossRef Medline

Churchland MM, Santhanam G, Shenoy KV (2006) Preparatory activity inpremotor and motor cortex reflects the speed of the upcoming reach.J Neurophysiol 96:3130 –3146. CrossRef Medline

Cicchini GM, Binda P, Burr DC, Morrone MC (2013) Transient spatiotopic

Tomassini et al. • Tactile Time Compression during Action J. Neurosci., July 2, 2014 • 34(27):9164 –9172 • 9171

integration across saccadic eye movements mediates visual stability.J Neurophysiol 109:1117–1125. CrossRef Medline

Coull JT, Vidal F, Nazarian B, Macar F (2004) Functional anatomy of theattentional modulation of time estimation. Science 303:1506 –1508.CrossRef Medline

Coull JT, Hwang HJ, Leyton M, Dagher A (2012) Dopamine precursor de-pletion impairs timing in healthy volunteers by attenuating activity inputamen and supplementary motor area. J Neurosci 32:16704 –16715.CrossRef Medline

Dassonville P (1995) Haptic localization and the internal representation ofthe hand in space. Exp Brain Res 106:434 – 448. Medline

Duhamel JR, Colby CL, Goldberg ME (1992) The updating of the represen-tation of visual space in parietal cortex by intended eye movements. Sci-ence 255:90 –92. CrossRef Medline

Eimer M, Van Velzen J, Gherri E, Press C (2006) Manual response prepara-tion and saccade programming are linked to attention shifts: ERP evi-dence for covert attentional orienting and spatially specific modulationsof visual processing. Brain Res 1105:7–19. CrossRef Medline

Forster B, Eimer M (2007) Covert unimanual response preparation triggersattention shifts to effectors rather than goal locations. Neurosci Lett 419:142–146. CrossRef Medline

Fraisse P (1984) Perception and estimation of time. Annu Rev Psychol 35:1–36. CrossRef Medline

Gibson JJ (1962) Observations on active touch. Psychol Rev 69:477– 491.CrossRef Medline

Haggard P, Clark S, Kalogeras J (2002) Voluntary action and consciousawareness. Nat Neurosci 5:382–385. CrossRef Medline

Hagura N, Kanai R, Orgs G, Haggard P (2012) Ready steady slow: actionpreparation slows the subjective passage of time. Proc Biol Sci 279:4399 –4406. CrossRef Medline

Helmholtz (1866) Concerning the perceptions in general. Treatise on phys-iological optics, Vol 3, Ed 3. J.P.C. Southall 1925 Opt Soc Am, Section 26.

Hermosillo R, Ritterband-Rosenbaum A, van Donkelaar P (2011) Predict-ing future sensorimotor states influences current temporal decision mak-ing. J Neurosci 31:10019 –10022. CrossRef Medline

Jackson SR, Parkinson A, Pears SL, Nam SH (2011) Effects of motor inten-tion on the perception of somatosensory events: a behavioural and func-tional magnetic resonance imaging study. Q J Exp Psychol (Hove) 64:839 – 854. CrossRef Medline

Juravle G, Deubel H (2009) Action preparation enhances the processing oftactile targets. Exp Brain Res 198:301–311. CrossRef Medline

Kitazawa S, Moizumi S, Okuzumi A, Saito F, Shibuya S, Takahashi T, WadaM, Yamamoto S (2008) Reversal of subjective temporal order due tosensory and motor integrations. In: Sensorimotor foundations of highercognition attention and performance XXII (Haggard P, et al., eds), pp73–97. Oxford: Oxford UP.

Lappe M, Awater H, Krekelberg B (2000) Postsaccadic visual referencesgenerate presaccadic compression of space. Nature 403:892– 895.CrossRef Medline

Lewis PA, Miall RC (2003) Brain activation patterns during measurement ofsub- and supra-second intervals. Neuropsychologia 41:1583–1592.CrossRef Medline

Macar F, Coull J, Vidal F (2006) The supplementary motor area in motorand perceptual time processing: fMRI studies. Cogn Process 7:89 –94.CrossRef Medline

Maij F, de Grave DD, Brenner E, Smeets JB (2011) Misjudging where youfelt a light switch in a dark room. Exp Brain Res 213:223–227. CrossRefMedline

Medendorp WP (2011) Spatial constancy mechanisms in motor control.Philos Trans R Soc Lond B Biol Sci 366:476 – 491. CrossRef Medline

Milne RJ, Aniss AM, Kay NE, Gandevia SC (1988) Reduction in perceivedintensity of cutaneous stimuli during movement: a quantitative study.Exp Brain Res 70:569 –576. Medline

Morrone MC, Ross J, Burr DC (1997) Apparent position of visual targetsduring real and simulated saccadic eye movements. J Neurosci 17:7941–7953. Medline

Morrone MC, Ross J, Burr D (2005) Saccadic eye movements cause com-pression of time as well as space. Nat Neurosci 8:950 –954. CrossRefMedline

Morrone MC, Cicchini M, Burr DC (2010) Spatial maps for time and mo-tion. Exp Brain Res 206:121–128. CrossRef Medline

Moscatelli A, Mezzetti M, Lacquaniti F (2012) Modeling psychophysicaldata at the population-level: the generalized linear mixed model. J Vis12(11):26 1–17. CrossRef Medline

Ostendorf F, Fischer C, Finke C, Ploner CJ (2007) Perisaccadic compressioncorrelates with saccadic peak velocity: differential association of eyemovement dynamics with perceptual mislocalization patterns. J Neurosci27:7559 –7563. CrossRef Medline

Post LJ, Zompa IC, Chapman CE (1994) Perception of vibrotactile stimuliduring motor activity in human subjects. Exp Brain Res 100:107–120.Medline

Ross J, Morrone MC, Burr DC (1997) Compression of visual space beforesaccades. Nature 386:598 – 601. CrossRef Medline

Rucci M, Iovin R, Poletti M, Santini F (2007) Miniature eye movementsenhance fine spatial detail. Nature 447:851– 854. CrossRef Medline

Shergill SS, Bays PM, Frith CD, Wolpert DM (2003) Two eyes for an eye: theneuroscience of force escalation. Science 301:187. CrossRef Medline

Sommer MA, Wurtz RH (2002) A pathway in primate brain for internalmonitoring of movements. Science 296:1480 –1482. CrossRef Medline

Teki S, Grube M, Kumar S, Griffiths TD (2011) Distinct neural substrates ofduration-based and beat-based auditory timing. J Neurosci 31:3805–3812. CrossRef Medline

Terao M, Watanabe J, Yagi A, Nishida S (2008) Reduction of stimulus visi-bility compresses apparent time intervals. Nat Neurosci 11:541–542.CrossRef Medline

Tomassini A, Gori M, Burr D, Sandini G, Morrone MC (2012) Active move-ment restores veridical event-timing after tactile adaptation. J Neuro-physiol 108:2092–2100. CrossRef Medline

Tse PU, Intriligator J, Rivest J, Cavanagh P (2004) Attention and the subjec-tive expansion of time. Percept Psychophys 66:1171–1189. CrossRefMedline

Vaziri S, Diedrichsen J, Shadmehr R (2006) Why does the brain predictsensory consequences of oculomotor commands? Optimal integration ofthe predicted and the actual sensory feedback. J Neurosci 26:4188 – 4197.CrossRef Medline

Wasaka T, Nakata H, Kida T, Kakigi R (2005) Changes in the centrifugalgating effect on somatosensory evoked potentials depending on the levelof contractile force. Exp Brain Res 166:118 –125. CrossRef Medline

Watanabe J, Nakatani M, Ando H, Tachi S (2009) Haptic localizations foronset and offset of vibro-tactile stimuli are dissociated. Exp Brain Res193:483– 489. CrossRef Medline

Williams SR, Chapman CE (2000) Time course and magnitude ofmovement-related gating of tactile detection in humans: II. Effects ofstimulus intensity. J Neurophysiol 84:863– 875. Medline

Williams SR, Chapman CE (2002) Time course and magnitude ofmovement-related gating of tactile detection in humans: III. Effect ofmotor tasks. J Neurophysiol 88:1968 –1979. Medline

Williams SR, Shenasa J, Chapman CE (1998) Time course and magnitude ofmovement-related gating of tactile detection in humans: I. Importance ofstimulus location. J Neurophysiol 79:947–963. Medline

Yamamoto S, Kitazawa S (2001a) Reversal of subjective temporal order dueto arm crossing. Nat Neurosci 4:759 –765. CrossRef Medline

Yamamoto S, Kitazawa S (2001b) Sensation at the tips of invisible tools. NatNeurosci 4:979 –980. CrossRef Medline

Yarrow K, Haggard P, Heal R, Brown P, Rothwell JC (2001) Illusory percep-tions of space and time preserve cross-saccadic perceptual continuity.Nature 414:302–305. CrossRef Medline

Yoshioka T, Craig JC, Beck GC, Hsiao SS (2011) Perceptual constancy oftexture roughness in the tactile system. J Neurosci 31:17603–17611.CrossRef Medline

9172 • J. Neurosci., July 2, 2014 • 34(27):9164 –9172 Tomassini et al. • Tactile Time Compression during Action